The Whole-Brain Concept of Death Remains Optimum

The Whole-Brain
Concept of Death
Remains Optimum
Public Policy
James L. Bernat
T
he definition of death is one of the oldest and
most enduring problems in biophilosophy and
bioethics. Serious controversies over formally
defining death began with the invention of the positive-pressure mechanical ventilator in the 1950s. For
the first time, physicians could maintain ventilation
and, hence, circulation on patients who had sustained
what had been previously lethal brain damage. Prior to
the development of mechanical ventilators, brain injuries severe enough to induce apnea quickly progressed
to cardiac arrest from hypoxemia. Before the 1950s,
the loss of spontaneous breathing and heartbeat (“vital
functions”) were perfect predictors of death because
the functioning of the brain and of all other organs
ceased rapidly and nearly simultaneously thereafter,
producing a unitary death phenomenon. In the pretechnological era, physicians and philosophers did not
have to consider whether a human being who had lost
certain “vital functions” but had retained others was
alive, because such cases were technically impossible.
With the advent of mechanical support of ventilation, (permitting maintenance of circulation) the previous unitary determination of death became ambiguous. Now patients were encountered in whom some
vital organ functions (brain) had ceased totally and
irreversibly, while other vital organ functions (such as
ventilation and circulation) could be maintained, albeit
mechanically. Their life status was ambiguous and debatable because they had features of both dead and living patients. They resembled dead patients in that they
could not move or breathe, were utterly unresponsive
to any stimuli, and had lost brain stem reflex activity.
But they also resembled living patients in that they had
maintained heartbeat, circulation and intact visceral
organ functioning. Were these unfortunate patients in
fact alive or dead?
In a series of scientific articles addressing this unprecedented state, several authors made the bold claim
that patients who had totally and irreversibly lost brain
functions were dead, despite their continued heartbeat and circulation.1 In the 1960s, they popularized
the concept they called “brain death” to acknowledge
this idea.2 The intuitive attractiveness of the concept of
“brain death” led to its rapid acceptance by the medical
and scientific community, and to legislators expeditiously drafting public laws permitting physicians to
determine death on the basis of loss of brain functioning.3 Interestingly, largely by virtue of its intuitive apJames L. Bernat, M.D., is Professor of Medicine (Neurology)
at Dartmouth Medical School and Director of the Clinical
Ethics Program at Dartmouth-Hitchcock Medical Center.
His most recent books are Ethical Issues in Neurology, 2nd
ed. (Butterworth-Heinemann, 2002) and Palliative Care in
Neurology (Oxford, 2004).
defining the beginning and the end of human life • spring 2006
35
SYMPOSIUM
peal, the academy, medical practitioners, governments,
and the public accepted the validity of brain death
prior to the development of a rigorous biophilosophical
proof that brain dead patients were truly dead. Medical
historians have emphasized utilitarian factors in this
rapid acceptance, because a determination of brain
death permitted the desired societal goals of cessation
of medical treatment and organ procurement.4
The practice of determining human death using
brain death tests has become worldwide over the past
several decades. The practice is enshrined in law in all
philosophical and medical task of determining the best
criterion of death, a measurable condition that shows
that the definition has been fulfilled by being both
necessary and sufficient for death; and (3) the medical-scientific task of determining the tests of death for
physicians to employ at the patient’s bedside to demonstrate that the criterion of death has been fulfilled with
no false positive and minimal false negative determinations. Most subsequent scholars have accepted this
method of analysis, if not our conclusions, with two
recent exceptions.12
Defining death is the conceptual task of making explicit our understanding
of it. It poses an essential question: what does it mean for an organism to die,
particularly in our contemporary circumstance in which technology
can compensate for the failure of certain vital organs?
50 states in the United States and in approximately 80
other countries, including nearly all of the developed
world and much of the undeveloped world.5 A 1995
conference on the definition of death sponsored by the
Institute of Medicine concluded that, despite certain
theoretical and practical shortcomings, the practice of
diagnosing brain death was so successful and so well
accepted by the medical profession and the public that
no major public policy changes seemed desirable.6
Yet despite this consensus, from its beginning, a persistent group of critics have attacked the concept and
practice of brain death as being conceptually invalid or
a violation of religious beliefs.7 Recently, through the
intellectual leadership of Alan Shewmon, additional
critics have concluded that the concept of brain death
is incoherent, anachronistic, unnecessary, a legal fiction, and should be abandoned.8 In this essay I show
that, despite admitted shortcomings, the classical formulation of whole-brain death remains both conceptually coherent and forms a solid foundation for public
policy surrounding human death determination and
organ transplantation.
An Analysis of Death
Defining death is a formidable task.9 In their rigorous, thoughtful, and highly influential book Defining
Death,10 the President’s Commission for the Study of
Ethical Problems in Medicine and Biomedical and Behavioral Research chose as their conceptual foundation
the analysis of death that I published with my Dartmouth colleagues Charles Culver and Bernard Gert.11
Our analysis was conducted in three sequential phases:
(1) the philosophical task of determining the definition
of death by making explicit the consensual concept of
death that has been confounded by technology; (2) the
36
Following a series of published critiques and rebuttals of our position over the past two decades, I concluded that much of the disagreement over our account of death resulted from the lack of acceptance
by dissenting scholars of the “paradigm of death.” By
“paradigm of death” I refer specifically to a set of conditions and assumptions that frame the discussion of the
topic of death by identifying the nature of the topic, the
class of phenomena to which it belongs, how it should
be discussed, and its conceptual boundaries.13 Accepting a paradigm of death permits scholars to rationally
analyze and discuss death without falling victim to the
fallacy of category noncongruence and consequently
talking past each other. But the paradigm remains useful even if scholars do not agree on all its elements,
because it can help clarify the root of their disagreement.
My paradigm of death comprises seven sequential
elements. First, the word “death” is a common, nontechnical word that we all use correctly to refer to the
cessation of a human being’s life. The philosophical
task of defining death seeks not to redefine it by contriving a new meaning, but rather to divine and make
explicit the implicit meaning of death that we all accept
but that has been made ambiguous by technological
advances. Some scholars have gone astray by not attempting to capture our consensual concept of death
and instead redefining death for ideological purposes
or by overanalyzing death to a metaphysical level of abstraction – thereby rendering it devoid of its ordinary
meaning.14
Second, death is fundamentally a biological phenomenon. We all agree that life is a biological entity; thus
also should be its cessation. Accepting that death is a
biological phenomenon neither denigrates the richness
journal of law, medicine & ethics
James L. Bernat
and beauty of various cultural and religious practices
surrounding death and dying, nor denies societies their
proper authority to govern practices and establish laws
regulating the determination and time of death. But
death is an immutable and objective biological fact
and not fundamentally a social contrivance.15 For the
definition and criterion of death, the paradigm thus
exclusively considers the ontology of death and ignores
its normative aspects.
Third, we restrict our analysis to the death of higher
vertebrate species for which death is univocal. That
is, we mean the same phenomenon of “death” when
we say our cousin died as we do when we say our dog
died. Although individual cells within organisms and
single celled organisms also die, our analysis of defining human death is simplified by restricting our purview to the death of related higher vertebrate species.
Determining the death of cells, organs, protozoa, or
bacteria are valid biophilosophical tasks but are not
the task at hand here.
Fourth, the term “death” can be applied directly and
categorically only to organisms. All living organisms
must die and only living organisms can die. Our use of
language may seem to confuse this point, for example,
when we say “a person died.” But by this usage we are
referring directly to the death of the living organism
that embodied the person, not to a living organism
ceasing to be a person. Personhood is a psychosocial
construct that can be lost but cannot die, except metaphorically. Similarly, other uses of the term “death”
such as “the death of a culture” clearly are metaphorical
and fall outside the paradigm.16
Fifth, a higher vertebrate organism can reside in only
one of two states, alive or dead: no organism can be in
both states or in neither. Based on the theory of fuzzy
sets, the concept that the world does not easily divide
itself into sets and their complements, Amir Halevy and
Baruch Brody proposed that an organism may reside in
a transitional state between alive and dead that shares
features of both states.17 This claim appears plausible
when considering cases of gradual, protracted dying, in
which it may be difficult and even appear arbitrary to
identify the precise moment of death. But this claim ignores the important distinction between our ability to
identify an organism’s biological state and the nature of
that state. Simply because we currently lack the technical ability to always accurately identify an organism’s
state does not necessitate postulating an in-between
state. Using the terminology of fuzzy set theory as a
guide, the paradigm requires us to view alive and dead
as mutually exclusive (non-overlapping) and jointly
exhaustive (no other) sets.
Sixth, and inevitably following from the preceding
premise, death must be an event and not a process.
If there are only two exclusive underlying states of an
organism, the transition from one state to the other,
at least in theory, must be sudden and instantaneous,
because of the absence of an intervening state. Disagreement on this point, highlighted since the original
debate over 30 years ago in Science by Robert Morison
and Leon Kass,18 centers on the difference between our
ability to accurately measure the presence of a biological state and the nature of that biological state. To an
observer, it may appear that death is an ineluctable
process within which it is arbitrary to stipulate the moment of death, but such an observation simply underscores our current technical limitations. For technical
reasons, the event of death may be determinable with
confidence only in retrospect. As my colleagues and I
first observed in 1981, death is best conceptualized not
as a process but as the event separating the biological
processes of dying and bodily disintegration.19
Seventh and finally, death is irreversible. By its nature, if the event of death were reversible it would not
be death but rather part of the process of dying that
was interrupted and reversed. Advances in technology permit physicians to interrupt the dying process in
some cases and postpone the event of death. So-called
“near-death experiences,” reported by some critically ill
patients who subsequently recovered, do not indicate
returning from the dead but are rather recalled experiences that result from alterations in brain physiology
during incipient dying that was reversed in a timely
manner.20
The Definition of Death
Given the set of assumptions and conditions comprising the paradigm of death, we can now explore the
definition, criterion, and tests of death. Defining death
is the conceptual task of making explicit our understanding of it. It poses an essential question: what does
it mean for an organism to die, particularly in our contemporary circumstance in which technology can compensate for the failure of certain vital organs?
We all agree that by “death” we do not require the cessation of functioning of every cell in the body, because
some integument cells that require little oxygen or
blood flow continue to function temporarily after death
is customarily declared. We also do not simply mean
the cessation of heartbeat and respiration, though this
circumstance will lead to death if untreated. Although
some religious believers assert that the soul departs the
body at the moment of death, this is not an adequate
definition of death because it is not what religious believers fundamentally mean by “death.”
Beginning early in the brain-death debate, Robert
Veatch advocated a position that became known as
the “higher-brain formulation of death.”21 He claimed
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37
SYMPOSIUM
that death should be defined formally as “the irreversible loss of that which is considered to be essentially
significant to the nature of man.” He expressly rejected
the idea that death should be related to an organism’s
“loss of the capacity to integrate bodily function” asserting that “man is, after all, something more than a
sophisticated computer.”22 His project attempted not
to reject brain death, but to refine the intuitive thinking underlying the brain death concept by emphasizing
that it was the cerebral cortex that counted in a brain
death concept and not the more primitive integrating
brain structures.
Irrespective of the attractiveness of this idea, (it has
spawned a loyal following23) the higher-brain formulation contains a fatal flaw as a candidate for a definition
of death: it is not what we mean when we say “death.”
Its logical criterion of death would be the irreversible
loss of consciousness and cognition, such as that which
occurs in patients in an irreversible persistent vegetative state (PVS). Thus a higher-brain formulation of
death would count PVS patients as dead. However, despite their profound and tragic disability, all societies,
cultures, and laws consider PVS patients as alive. Thus,
despite its potential merits, the higher-brain formulation fails the first condition of the paradigm: to make
explicit our underlying consensual concept of death
and not to contrive a new definition of death.
In 1981, my colleagues and I strove to capture the
essence of the concept of human death that formed
the intuitive foundation of the brain-based criterion
of death. We defined death as “the cessation of functioning of the organism as a whole.”24 This definition
utilized a biological concept proposed by Jacques Loeb
in 1916.25 Loeb explained that organisms are not simply
composites of cells, tissues, and organs, but possess
overarching functions that regulate and integrate all
systems to maintain the unity and interrelatedness of
the organism to promote its optimal functioning and
health. The organism as a whole comprises that set of
functions that are greater than the mere sum of the
organism’s parts.
More recently, biophilosophers have advanced the
concept of “emergent functions” to explain this type
of phenomenon with greater conceptual clarity.26 An
emergent function is a property of a whole that is not
possessed by any of its component parts, and that cannot be reduced to one or more of its component parts.
The physiological correlate of the organism as a whole
is the set of emergent functions of the organism. The
irretrievable loss of the organism’s emergent functions
produces loss of the critical functioning of the organism as a whole and therefore is the death of the organism.
38
In early writings on brain death, a few scholars
proposed similar ideas. Most noteworthy was Julius
Korein who asserted that the brain was the “critical system” of the organism whose loss indicated the
organism’s death.27 Using thermodynamics theory,
Korein argued that once the critical system was irretrievably lost (death), an irreversible and unstoppable
process ensued of increasing entropy that constituted
the process of bodily disintegration. The concept of
the demise of the organism’s critical system relies on
concepts analogous to the cessation of functions of the
organism as a whole.
Examples of critical functions of the organism as a
whole include: (1) consciousness, which is necessary
for the organism to respond to requirements for hydration and nutrition; (2) control of circulation, respiration, and temperature control, which are necessary for
all cellular metabolism; and (3) integrating and control
systems involving chemoreceptors, baroreceptors, and
neuroendocrine feedback loops to maintain homeostasis. Death is the irreversible and permanent loss of the
critical functions of the organism as a whole.
The Criterion of Death
The next task is to identify the criterion of death, the
general measurable condition that satisfies the definition of death by being both necessary and sufficient
for death. There are several plausible candidates for a
criterion of death. Among brain death advocates, three
separate criteria have been proposed: (1) the wholebrain formulation, the criterion recommended by the
Harvard Committee and the President’s Commission,
and accepted throughout the United States and in most
parts of the world; (2) the higher-brain formulation,
popular in the academy but accepted in no jurisdictions anywhere; and (3) the brain stem formulation
accepted in the United Kingdom.28
The whole-brain criterion requires cessation of all
brain clinical functions including those of the cerebral
hemispheres, diencephalon (thalamus and hypothalamus), and brain stem. Whole-brain theorists require
widespread cessation of neuronal functions because
each part of the brain serves the critical functions of
the organism as a whole. The brain stem initiates and
controls breathing, regulates circulation, and serves as
the generator of conscious awareness through the ascending reticular activating system. The diencephalon
provides the center for bodily homeostasis, regulating
and coordinating numerous neuroendocrine control
systems such as those regulating body temperature,
salt and water regulation, feeding behavior, and memory. The cerebral hemispheres have an indispensable
role in awareness that provides the conditions for all
journal of law, medicine & ethics
James L. Bernat
conscious behavior that serves the health and survival
reticular activating system), have continued control
of the organism.
of respiration and circulation by the intact medulla,
Clinical functions are those that are measurable at
and retain other brain stem mediated regulatory functhe bedside. The distinction between the brain’s clinitions.34 The higher-brain formulation, thus, serves as
cal functions and brain activities, recordable electrineither an adequate definition nor criterion of death.
cally or though other laboratory means, was made by
The criterion of the brain stem formulation is the
the President’s Commission in Defining Death though,
loss of consciousness and the capacity for breathing.35
for the sake of brevity, it did not appear in the Uniform
Diffuse damage to the brain stem that is sufficient to
Determination of Death Act proposed by the Commisdestroy the ascending reticular activating system and
sion.29 All clinical brain functions measurable at the
the medullary breathing center satisfies this criterion.
bedside must be lost and the absence must be shown to
But the brain stem formulation does not require combe irreversible. But the whole-brain criterion does not
mensurate damage to the diencephalon or cerebral
require the loss of all neuronal activities. Some neurons
hemispheres. It therefore leaves open the possibility of
may survive and contribute to recordable brain activimisdiagnosis of death because of a pathological process
ties (by an electroencephalogram, for example) but not
that appears to destroy brain stem activities but that
to clinical functions.30 The precise number, location,
permits some form of residual conscious awareness
and configuration of the minimum number of critical
that cannot be easily detected. It thus lacks the fail-safe
neuron arrays remain unknown.
Despite the fact that the whole-brain
The higher-brain formulation fails to provide
criterion does not require the cessation of
an adequate criterion of death because its
functioning of every brain neuron, it does
rely on a pathophysiological process known
conditions are insufficient for the loss of the
as brain herniation to assure widespread
critical functions of the organism as a whole.
destruction of the neuron systems responsible for the brain’s clinical functions.31
When the brain is injured diffusely by trauma, hypoxicfeature of whole-brain death to test for and guarantee
ischemic damage during cardiorespiratory arrest or asthe irreversible loss of these critical systems.
As a criterion of death, the circulation formulation
phyxia, meningoencephalitis, or enlarging intracranial
32
fails
for precisely the opposite reason of the highermass lesions such as neoplasms, brain edema causes
brain
and brain stem formulations. Whereas the
intracranial pressure to rise to levels exceeding mean
higher-brain
and brain stem criteria both fail because
arterial blood pressure. At this point, intracranial cirthey
are
necessary
but not sufficient for death, the circulation ceases and nearly all brain neurons that were
culation
criterion
fails
because it is sufficient but not
not destroyed by the initial brain injury are secondarily
necessary
for
death.
The
loss of all systemic circulation
destroyed by lack of intracranial circulation. Thus the
whole-brain formulation provides a fail-safe mechaproduces the destruction of all bodily organs and tisnism to eliminate false-positive brain death determisues so it is clearly a sufficient condition for death. But
nations and assure the loss of the critical functions of
it is unnecessary to require the cessation of functions
the organism as a whole. Showing the absence of all inof organs that do not serve the critical functions of the
tracranial circulation is sufficient to prove widespread
organism as a whole.36
destruction of all critical neuronal systems. Similarly,
it satisfies Korein’s requirement for the loss of the irThe Tests of Death
replaceable critical system of the organism.
Brain death tests must be used to determine death only
The higher-brain formulation fails to provide an adin the unusual case in which a patient’s ventilation is
equate criterion of death because its conditions are
being supported. If positive-pressure ventilation is neiinsufficient for the loss of the critical functions of the
ther employed nor entertained, the traditional tests of
organism as a whole. Its criterion is the irreversible
death – prolonged absence of breathing and heartbeat
loss of consciousness and cognition. The most com– can be used successfully. These traditional tests are
mon clinical manifestation of this condition is the PVS,
absolutely predictive that the brain will be rapidly decaused by diffuse damage to the cerebral hemispheres,
stroyed by lack of blood flow and oxygen, at which time
thalami, or disconnections between those structures.33
death will have occurred. Traditional examinations for
In most cases of PVS, brain stem neurons and their
death, in addition to testing for heartbeat and breathfunctions remain intact, so PVS patients, although
ing, always included tests for responsiveness and pupilunaware, have retained wakefulness and sleep-wake
lary reflexes that directly measure brain function.
cycles (through the function of the intact ascending
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39
SYMPOSIUM
The bedside tests satisfying the whole-brain criterion
of death have been designed with a sufficiently high
degree of concordance to permit the drafting of widely
accepted clinical practice guidelines on the determination of brain death.37 The tests require demonstrating
the loss of all clinical brain functions, irreversibility,
and a known structural process sufficient to produce
the clinical findings. Laboratory tests showing the absence of intracranial blood flow or the absence of electrical activity in the hemispheres and brain stem can
be used to confirm the clinical diagnosis to expedite
the determination.38
Irreversibility is an indispensable requirement for
brain death. There is general belief that irreversibility
can be adequately demonstrated by conducting serial
neurological examinations, excluding potentially reversible factors, and demonstrating a structural cause
that is sufficient to account for the clinical signs. But,
while highly plausible, these conditions have never
been proved to assure irreversibility. Two recent factors prompted me to reassess my previous position that
irreversibility could be proved solely by clinical factors
and to suggest that a laboratory test showing cessation
of all intracranial blood flow should become mandatory in brain death determination.
There are several published studies documenting the
alarming frequency of physician variations and errors
in performing brain death tests,39 despite clear guidelines for performing and recording the tests. Patients
with “chronic brain death” have been reported who
were diagnosed as brain dead but whose circulation
and visceral organ functioning were successfully physiologically maintained for months or longer.40 Eelco
Wijdicks and I questioned whether all of the reported
patients were correctly diagnosed, and if some braindamaged but not brain dead patients were included
because of inadequate examinations and resultant incorrect brain death determinations.41 Reacting to both
these findings, I proposed that the mere assertion of
irreversibility may no longer be sufficient to diagnose
brain death and that a test showing cessation of all
intracranial blood flow, such as transcranial Doppler
ultrasonography, radionuclide angiography, or computed tomographic angiography, should become mandatory, at least if there is any question about the diagnosis or if the examiner is inexperienced.42
Public Policy on Death
Brain death is widely regarded as the prime example of
a formerly contentious bioethical and biophilosophical
issue that has been resolved to the point of widespread
public consensus.43 Evidence for this consensus is the
enactment of effective and well-accepted brain death
laws and policies throughout the world.44 In the United
40
States, the Uniform Determination of Death Act, recommended by the President’s Commission and the National Conference of Commissioners on Uniform State
Laws,45 has been enacted in most states, and others
have enacted statutes with similar language. Contemporaneously, the Law Reform Commission of Canada
produced a similar statute.46
But an observer unaware of this consensus and public acceptance, who relied solely on reading the output of scholarly articles and university conferences on
brain death, would reach a far different conclusion. The
publication of anti-brain death articles has never been
greater than during the past decade. Yet, despite those
arguments, the 1995 Institute of Medicine conference
on brain death recommended no changes in public
laws in the United States,47 no jurisdiction has abandoned its brain death statute, and there is evidence that
many additional countries have embraced the practice
of determining brain death during the past decade of
scholarly dissention.48 What accounts for the mismatch
between public acceptance and scholarly agitation?
Higher-brain proponents continue to accept brain
death but argue that the criterion of death should be
changed to the higher-brain formulation. Brain stem
death proponents also accept the conceptual validity of
brain death but hold that the criterion of death should
be the brain stem formulation. Religious authorities
continue a debate that has raged for 40 years about
whether brain death is compatible with the doctrines
of the world’s principal religious traditions.49 Protestantism, including fundamentalism, has accepted
brain death.50 The debate in Roman Catholicism was
largely settled by Pope John Paul’s 2000 pronouncement embracing brain death as consistent with Catholic teachings.51 In Judaism, brain death is accepted by
Reform and Conservative authorities, but an Orthodox
rabbinic debate continues between those who declare
brain death compatible with Jewish law and those who
do not.52 Brain death determination is also practiced
in several Islamic societies,53 Hindi societies,54 and in
Confucian-Shinto Japan.55
The principal active opponents within the academy
are those who reject the concept of brain death outright and promote the concept that a human being is
not dead until the systemic circulation ceases and all
organs are destroyed. The circulation proponents see
no special role for brain functions in a determination
of death. Alan Shewmon, the intellectual leader of the
circulationists, has written eloquently on the conceptual problems inherent within the whole-brain (or any
brain criterion) formulation.56 He cites evidence that
the brain performs no qualitatively different forms
of integration than the spinal cord and argues that
therefore it should enjoy no special status above other
journal of law, medicine & ethics
James L. Bernat
organs in death determination. He claims further that
his cases of “chronic brain death” show that the concept
of brain death is inherently counterintuitive, for how
could a dead body gestate infants or grow?57
Another critic, Robert Taylor, has called the brain
death concept a “legal fiction” that is accepted by society in a manner analogous to the concept of legal blindness. Taylor explains that legal blindness is a concept
invented by society to permit people who are functionally blind from severe visual impairment to receive the
same social benefits as those enjoyed by people who
are totally blind. We all know that most people who
are declared legally blind are not truly blind. But we
employ a legal fiction and use the term “blindness” in
a biologically incorrect way for its socially beneficial
purpose. Taylor argues that, by analogy, we know that
people we declare “brain dead” are not truly dead, but
we consider them dead for the socially beneficial goal
of organ procurement.58
As a longstanding proponent of whole-brain death,
I acknowledge that the whole-brain formulation, although coherent, is imperfect, and that my attempts
to defend it have not adequately addressed all valid
criticisms. But my inadequacies must be viewed within
the larger context of the relationship of biology to public policy. Our attempts to conceptualize, understand,
and define the complex and subtle natural concepts of
life and death remain far from perfect. Perhaps we will
never be able to achieve uniform definitions of life and
death that everyone accepts and that no one criticizes
for conceptual or practical shortcomings.
In the real world of public policy on biological issues, we must frequently make compromises or approximations to achieve acceptable practices and laws.
For these compromises to be tolerable, generally they
should be minor and not affect outcomes. For example,
in the current practice of organ donation after cardiac
death (formerly known as non-heart-beating organ
donation), I and others raised the question of whether
the organ donor patients were truly dead after only five
minutes of asystole. The five-minute rule was accepted
by the Institute of Medicine as the point at which death
could be declared and the organs procured.59 Ours was
a biologically valid criticism because, at least in theory,
some such patients could be resuscitated after five minutes of asystole and still retain measurable brain function. If that was true, they were not yet dead at that
point so their death declaration was premature.
But thereafter I changed my position to support programs of organ donation after cardiac death. I decided
that it was justified to accept a compromise on this biological point when I realized that donor patients, if not
already dead at five minutes of asystole, were incipiently
and irreversibly dying because they could not auto-re-
suscitate and no one would attempt their resuscitation.
Because their loss of circulatory and respiratory functions was permanent if not yet irreversible, there would
be no difference whatsoever in their outcomes if their
death were declared after five minutes of asystole or
after 60 minutes of asystole. I concluded that, from a
public policy perspective, accepting the permanent loss
of circulatory and respiratory functions rather than
requiring their irreversible loss was justified. The good
accruing to the organ recipient, the donor patient, and
the donor family resulting from organ donation justified overlooking the biological shortcoming because,
although the difference in the death criteria was real,
it was inconsequential.
Of course Alan Shewmon is correct that not all bodily
system integration and functions of the organism as a
whole are conducted by the brain (though most are)
and that the spinal cord and other structures serve
relevant roles. And Robert Taylor is correct that many
people view brain death as a legal fiction and regard
such patients “as good as dead” but not biologically
dead. But despite its shortcomings, the whole-brain
formulation remains coherent on the grounds of the
critical functions of the organism as a whole and on the
additional grounds of Korein’s critical system theory.
The whole-brain death formulation comprises a concept and public policy that make intuitive and practical sense and have been well accepted by the public
throughout many societies. Therefore, while I am willing to acknowledge that whole-brain death formulation
remains imperfect, I continue to support it because on
the public policy level its shortcomings are relatively
inconsequential.
Those scholars attacking the established wholebrain death formulation have a duty to show that their
proposed alternative formulations not only more accurately represent biological reality, but also can be
translated into successful public policy that is intuitively acceptable and maintains public confidence in
physicians’ accuracy in death determination and in
the integrity of the organ procurement enterprise. Although I acknowledge certain weakness of the wholebrain death formulation, I hold that it most accurately
maps our consensual implicit concept of death in a
technological age and, as a consequence, it has been
accepted by societies throughout the world.
References
1. The early history of “brain death” is discussed in M. S. Pernick,
“Brain Death in a Cultural Context: The Reconstruction of Death
1967-1981,” in S. J. Youngner, R. M. Arnold, and R. Schapiro, eds.,
The Definition of Death: Contemporary Controversies (Baltimore:
Johns Hopkins University Press, 1999): 13-33; and M. N. Diringer
and E. F. M. Wijdicks, “Brain Death in Historical Perspective,”
in E. F. M. Wijdicks, ed., Brain Death (Philadelphia: Lippincott
Williams & Wilkins, 2001): 5-27. Early reports from France de-
defining the beginning and the end of human life • spring 2006
41
SYMPOSIUM
scribed coma dépassé (a state beyond coma). See P. Mollaret and
M. Goulon, “Le Coma Dépassé (Mémoire Préliminaire)” Revue
Neurologique 101 (1959): 3-15. The Harvard Medical School report
was the earliest widely publicized article to claim that such patients
were dead. See “A Definition of Irreversible Coma: Report of the
Ad Hoc Committee of the Harvard Medical School to Examine the
Definition of Brain Death,” JAMA 205 (1968): 337-340.
2. “Brain death” is the colloquial term for human death determination using tests of absent brain functions. But it is an unfortunate
term because it is inherently misleading. It falsely implies that
there are two types of death: brain death and ordinary death, instead of unitary death tested using two sets of tests. It also wrongly
suggests that only the brain is dead in such patients. Robert Veatch
stated that because of these shortcomings he uses the term only in
quotation marks (personal communication November 4, 1995).
3. In 1970, Kansas became the first state to enact a death statute
incorporating the new concept of brain death, a mere two years
after the Harvard Medical School report. See I. M. Kennedy, “The
Kansas Statute on Death – An Appraisal,” New England Journal
of Medicine 285 (1971): 946-950, at 946.
4. See G. S. Belkin, “Brain Death and the Historical Understanding
of Bioethics,” Bulletin of the History of Medical Allied Sciences 58
(2003): 325-361; E. F. M. Wijdicks, “The Neurologist and Harvard
Criteria for Brain Death,” Neurology 61 (2003): 970-976; M. Giacomini, “A Change of Heart and a Change of Mind? Technology
and the Redefinition of Death in 1968,” Social Science & Medicine
44 (1997): 1465-1482; and M. S. Pernick, supra note 1.
5. In nearly all states, brain death is incorporated into the statute of
death. In a few jurisdictions, brain death is permitted in administrative regulations. See H. R. Beresford, “Brain Death,” Neurologic
Clinics 17 (1999): 295-306. For international practices of brain
death, see E. F. M. Wijdicks, “Brain Death Worldwide: Accepted
Fact but No Global Consensus in Diagnostic Criteria,” Neurology
58 (2002): 20-25.
6. S. J. Youngner, R. M. Arnold, and R. Schapiro, eds., The Definition
of Death: Contemporary Controversies (Baltimore: Johns Hopkins
University Press, 1999).
7. See, for example, R. D. Truog, “Is it Time to Abandon Brain Death?”
Hastings Center Report 27, no. 1 (1997): 29-37; R. M. Taylor, “Reexamining the Definition and Criterion of Death,” Seminars in
Neurology 17 (1997): 265-270; P. A. Byrne, S. O’Reilly, and P. M.
Quay, “Brain Death – An Opposing Viewpoint,” JAMA 242 (1979):
1985-1990; and J. Seifert, “Is Brain Death Actually Death? A Critique of Redefinition of Man’s Death in Terms of ‘Brain Death,’”
The Monist 76 (1993): 175-202.
8. Alan Shewmon’s recent works on this topic include D. A. Shewmon, “The Brain and Somatic Integration: Insights into the Standard Biological Rationale for Equating ‘Brain Death’ with Death,”
Journal of Medicine and Philosophy 26 (2001): 457-478; and D.
A. Shewmon, “The ‘Critical Organ’ for the Organism as a Whole:
Lessons from the Lowly Spinal Cord,” Advances in Experimental
Medicine and Biology 550 (2004): 23-42. Other scholars agreeing
with him also published works following his article in the Journal
of Medicine and Philosophy.
9. H. K. Beecher, chairman of the landmark 1968 Harvard Medical School Committee report (see note 1), later warned: “Only a
very bold man, I think, would attempt to define death.” See H.
K. Beecher, “Definitions of ‘Life’ and ‘Death’ for Medical Science
and Practice,” Annals of the New York Academy of Sciences 169
(1970): 471-474.
10. President’s Commission for the Study of Ethical Problems in
Medicine and Biomedical and Behavioral Research, Defining
Death: Medical, Legal and Ethical Issues in the Determination
of Death (Washington, DC: U.S. Government Printing Office,
1981): at 31-43.
11. J. L. Bernat, C. M. Culver and B. Gert, “On the Definition and
Criterion of Death,” Annals of Internal Medicine 94 (1981): 389394.
12. Alan and Elisabeth Shewmon recently claimed that my approach
is futile because language constrains our capacity to conceptualize life and death. They regard death as an “ur-phenomenon” that
is “…conceptually fundamental in its class; no more basic con-
42
cepts exist to which it can be reduced. It can only be intuited from
our experience of it…” See D. A. Shewmon and E. S. Shewmon,
“The Semiotics of Death and its Medical Implications,” Advances
in Experimental Medicine and Biology 550 (2004): 89-114. Winston Chiong also rejected my analytic approach claiming that
there can be no unified definition of death. Yet, he agreed that
the whole-brain criterion of death is the most coherent concept
of death. See W. Chiong, “Brain Death Without Definitions,”
Hastings Center Report 35 (2005): 20-30.
13. I have discussed these conditions in greater detail in J. L. Bernat,
“The Biophilosophical Basis of Whole-Brain Death,” Social Philosophy & Policy 19, no. 2 (2002): 324-342.
14. Robert Veatch exemplifies a scholar who has attempted to redefine death for the purpose of considering patients in persistent
vegetative states as dead, despite the fact that all societies consider them alive. See, for example, R. M. Veatch, “The Impending Collapse of the Whole-Brain Definition of Death,” Hastings
Center Report 23, no. 4 (1993): 18-24. Linda Emanuel abstracted
death to a clinically unhelpful metaphysical level: “there is no
state of death…to say ‘she is dead’ is meaningless because ‘she’
is not compatible with ‘dead.’” See L. L. Emanuel, “Reexamining
Death: The Asymptotic Model and a Bounded Zone Definition,”
Hastings Center Report 25, no. 4 (1995): 27-35.
15. For a scholar who argues that the definition of death is largely
a normative social matter, see R. M. Veatch, “The Conscience
Clause: How Much Individual Choice in Defining Death Can Our
Society Tolerate?” in S. J. Youngner, R. M. Arnold, and R. Schapiro, eds., The Definition of Death: Contemporary Controversies
(Baltimore: Johns Hopkins University Press, 1999): 137-160.
16. In this regard, I disagree with Jeff McMahon that there are two
types of death: death of the organism and death of the person.
See J. McMahon, “The Metaphysics of Brain Death,” Bioethics
9 (1995): 91-126.
17. A. Halevy and B. Brody, “Brain Death: Reconciling Definitions,
Criteria, and Tests,” Annals of Internal Medicine 119 (1993): 519525.
18. R. S. Morison, “Death: Process or Event?” Science 173 (1971):
694-698 and L. Kass, “Death as an Event: A Commentary on
Robert Morison,” Science 173 (1971): 698-702. The Shewmons
(see note 12) recently described the process vs. event argument
as “tiresome” because, as a consequence of linguistic constraints,
death can be understood only as an event.
19. J. L. Bernat, C. M. Culver, and B. Gert, “On the Definition and
Criterion of Death,” Annals of Internal Medicine 94 (1981): 389394.
20. S. Parnia, D. G. Waller, R. Yeates, and P. Fenwick, “A Qualitative
and Quantitative Study of the Incidence, Features, and Etiology
of Near Death Experiences in Cardiac Arrest Survivors,” Resuscitation 48 (2001): 149-156.
21. R. M. Veatch, “The Whole Brain-Oriented Concept of Death: An
Outmoded Philosophical Formulation,” Journal of Thanatology 3 (1975): 13-30; R. M. Veatch, “Brain Death and Slippery
Slopes,” Journal of Clinical Ethics 3 (1992): 181-187; and R. M.
Veatch, “The Impending Collapse of the Whole-Brain Definition
of Death,” Hastings Center Report 23, no. 4 (1993): 18-24.
22. R. M. Veatch, supra note 21, at 23.
23. See, for example, M. B. Green and D. Wikler, “Brain Death and
Personal Identity,” Philosophy and Public Affairs 9 (1980): 105133; S. J. Youngner and E. T. Bartlett, “Human Death and High
Technology: The Failure of the Whole Brain Formulation,” Annals of Internal Medicine 99 (1983): 252-258; and K. G. Gervais,
Redefining Death (New Haven: Yale University Press, 1986).
24. J. L. Bernat, C. M. Culver, and B. Gert, “On the Definition and
Criterion of Death,” Annals of Internal Medicine 94 (1981): 389394. I later refined the definition to require only the permanent
loss of the critical functions of the organism as a whole, in response to exceptional cases raised, but this is mostly quibbling.
See J. L. Bernat, “Refinements in the Definition and Criterion
of Death,” in S. J. Youngner, R. M. Arnold, and R. Schapiro,
eds., The Definition of Death: Contemporary Controversies (Baltimore: Johns Hopkins University Press, 1999): 83-92.
journal of law, medicine & ethics
James L. Bernat
25. J. Loeb, The Organism as a Whole (New York: G. P. Putnam’s
Sons, 1916).
26. See, for example, the explanation of emergent functions in M.
Mahner and M. Bunge, Foundations of Biophilosophy (Berlin:
Springer-Verlag, 1997): at 29-30.
27. J. Korein, “The Problem of Brain Death: Development and History,” Annals of the New York Academy of Sciences 315 (1978):
19-38. For the most recent refinement of Korein’s argument, see
J. Korein and C. Machado, “Brain Death: Updating a Valid Concept for 2004,” Advances in Experimental Medicine and Biology
550 (2004): 1-14.
28. I have discussed these three formulations in greater detail in J.
L. Bernat, “How Much of the Brain Must Die in Brain Death?”
Journal of Clinical Ethics 3 (1992): 21-26.
29. The text of Defining Death makes clear that the President’s Commission found an important distinction between brain clinical
functions and brain activities. See President’s Commission for
the Study of Ethical Problems in Medicine and Biomedical and
Behavioral Research, Defining Death: Medical, Legal and Ethical Issues in the Determination of Death (Washington, DC: U.S.
Government Printing Office, 1981): at 28-29.
30. Residual EEG activity seen on unequivocally brain dead patients
has been described by M. M. Grigg, M. A. Kelly, G. G. Celesia, M.
W. Ghobrial, and E. R. Ross, “Electroencephalographic Activity
after Brain Death,” Archives of Neurology 44 (1987): 948-954.
31. F. Plum and J. B. Posner, The Diagnosis of Stupor and Coma, 3rd
ed., (Philadelphia: F. A. Davis, 1980): at 88-101.
32. These are the most common causes of brain death. See D.
Staworn, L. Lewison, J. Marks, G. Turner, and D. Levin, “Brain
Death in Pediatric Intensive Care Unit Patients: Incidence, Primary Diagnosis, and the Clinical Occurrence of Turner’s Triad,”
Critical Care Medicine 22 (1994): 1301-1305.
33. H. C. Kinney and M. A. Samuels, “Neuropathology of the Persistent Vegetative State: A Review,” Journal of Neuropathology and
Experimental Neurology 53 (1994): 548-558.
34. Multi-Society Task Force on PVS, “Medical Aspects of the Persistent Vegetative State. Parts I and II,” New England Journal of
Medicine 330 (1994): 1499-1508, 1572-1579.
35. Conference of Medical Royal Colleges and their Faculties in the
United Kingdom, “Diagnosis of Brain Death,” British Medical
Journal 2 (1976): 1187-1188; and C. Pallis, ABC of Brainstem
Death (London: British Medical Journal Publishers, 1983).
36. I have provided more extensive arguments with examples to
support this claim in J. L. Bernat, “A Defense of the Whole-Brain
Concept of Death,” Hastings Center Report 28, no. 2 (1998): 1423 at 18-19.
37. The Quality Standards Subcommittee of the American Academy of Neurology, “Practice Parameters for Determining Brain
Death in Adults [Summary Statement],” Neurology 45 (1995):
1012-1014. The tests accepted in various European countries are
described and compared in W. F. Haupt and J. Rudolf, “European Brain Death Codes: A Comparison of National Guidelines,”
Journal of Neurology 246 (1999): 432-437.
38. The clinical and confirmatory tests for brain death are described
in detail in E. F. M. Wijdicks, “The Diagnosis of Brain Death,”
New England Journal of Medicine 344 (2001): 1215-1221.
39. See, for example, R. E. Mejia and M. M. Pollack, “Variability in
Brain Death Determination Practices in Children,” JAMA 274
(1995): 550-553; and M. Y. Wang, P. Wallace, and J. B. Gruen,
“Brain Death Documentation: Analysis and Issues,” Neurosurgery 51 (2002): 731-735.
40. D. A. Shewmon, “Chronic ‘Brain Death’: Meta-analysis and Conceptual Consequences,” Neurology 51 (1998): 1538-1545.
41. E. F. M. Wijdicks and J. L. Bernat, “Chronic ‘Brain Death’: Metaanalysis and Conceptual Consequences,” (letter to the editor)
Neurology 53 (1999): 1639-1640.
42. I defend this claim in J. L. Bernat, “On Irreversibility as a Prerequisite for Brain Death Determination,” Advances in Experimental Medicine and Biology 550 (2004): 161-167.
43. This conclusion was reached by Alexander Capron, the former
Executive Director of the President’s Commission (see note 10),
in A. M. Capron, “Brain Death – Well Settled Yet Still Unresolved,” New England Journal of Medicine 344 (2001): 12441246.
44. E. F. M. Wijdicks, “Brain Death Worldwide: Accepted Fact but
No Global Consensus in Diagnostic Criteria,” Neurology 58
(2002): 20-25.
45. President’s Commission for the Study of Ethical Problems in
Medicine and Biomedical and Behavioral Research, Defining
Death: Medical, Legal and Ethical Issues in the Determination
of Death (Washington, DC: U.S. Government Printing Office,
1981): at 72-84.
46. Law Reform Commission of Canada, Criteria for the Determination of Death (Ottawa: Law Reform Commission of Canada,
1981).
47. R. A. Burt, “Where Do We Go from Here?” in S. J. Youngner, R.
M. Arnold, and R. Schapiro, eds., The Definition of Death: Contemporary Controversies (Baltimore: Johns Hopkins University
Press, 1999): 332-339.
48. See E. F. M. Wijdicks, supra note 5, at 22-23.
49. In the early brain death era, commentators asserted that brain
death was compatible with the world’s principal religions. See F.
J. Veith, J. M. Fein, M. D. Tendler, R. M. Veatch, M. A. Kleiman,
and G. Kalkines, “Brain Death: I. A Status Report of Medical and
Ethical Considerations,” JAMA 238 (1977): 1651-1655.
50. C. S. Campbell, “Fundamentals of Life and Death: Christian
Fundamentalism and Medical Science,” in S. J. Youngner, R.
M. Arnold, and R. Schapiro, eds., The Definition of Death: Contemporary Controversies (Baltimore: Johns Hopkins University
Press, 1999): 194-209.
51. Some Catholic commentators had long claimed that brain death
violated Catholic teachings. See P. A. Byrne, et al., supra note
7. But in August, 2000, in an address to the 18th Congress of
the International Transplantation Society meeting in Rome, the
Pope asserted that brain death was fully consistent with Catholic doctrine. For a detailed historical discussion of earlier statements on brain death from Vatican academies, an account of the
process of Vatican decision making, and an explanation of the
Pope’s recent statement, see E. J. Furton, “Brain Death, the Soul,
and Organic Life,” The National Catholic Bioethics Quarterly 2
(2002): 455-470.
52. The rabbinic debate is explained in F. Rosner, “The Definition
of Death in Jewish Law,” in S. J. Youngner, R. M. Arnold, and
R. Schapiro, eds., The Definition of Death: Contemporary Controversies (Baltimore: Johns Hopkins University Press, 1999):
210-221.
53. Saudi Arabia represents a conservative interpretation of Islam
and brain death is accepted there. See B. A. Yaqub and S. M.
Al-Deeb, “Brain Death: Current Status in Saudi Arabia,” Saudi
Medical Journal 17 (1996): 5-10.
54. S. Jain and M. C. Maheshawari, “Brain Death – The Indian Perspective,” in C. Machado, ed., Brain Death (Amsterdam: Elsevier,
1995): 261-263.
55. M. Lock, “Contesting the Natural in Japan: Moral Dilemmas
and Technologies of Dying,” Culture, Medicine and Psychiatry
19 (1995): 1-38.
56. See Shewmon, supra note 8.
57. See Shewmon, supra note 40.
58. R. M. Taylor, “Re-examining the Definition and Criterion of
Death,” Seminars in Neurology 17 (1997): 265-270.
59. I made this point in a review of a pre-publication draft of the
Institute of Medicine report. See, Institute of Medicine, NonHeart-Beating Organ Transplantation: Practice and Protocols
(Washington DC: National Academy Press, 2000): at 22-24. The
same point was made in reference to an earlier publication of the
Institute of Medicine in J. Menikoff, “Doubts about Death: The
Silence of the Institute of Medicine,” Journal of Law, Medicine
& Ethics 26 (1998): 157-165.
defining the beginning and the end of human life • spring 2006
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